Introduction

Midgut malrotation is defined as congenital abnormal rotation of the midgut about the axis of the superior mesenteric artery (SMA) [1, 2]. Malrotation can be complicated by volvulus, a surgical emergency that can lead to bowel infarction if not promptly treated [3, 4]. This pictorial essay describes the US technique and findings of complicated midgut malrotation, specifically by volvulus.

Epidemiology and clinical presentation

Malrotation occurs in 3.9 per 10,000 live births [5], although this is likely an underestimation because asymptomatic cases might go undiagnosed. Symptomatic midgut malrotation caused by midgut volvulus or Ladd bands typically presents early in life, with 58.2% in the first year after birth and 75% before the age of 5 years [6].

The most common clinical presentation of malrotation complicated by midgut volvulus or Ladd bands in infants is bilious emesis, although 20–35% of vomitus is not initially bile-stained [7, 8]. Older children and adults might have more nonspecific symptoms such as abdominal pain [9,10,11].

Why ultrasound for midgut malrotation and volvulus?

Reported frequencies of bowel necrosis and mortality from midgut volvulus are 9.3–17.6% and 5.6–15.3%, respectively [3, 12, 13]. These numbers indicate that midgut volvulus is life-threatening and requires prompt and accurate diagnosis. To be most effective, a diagnostic imaging test for midgut volvulus should have high sensitivity and specificity. US has been shown to have a sensitivity of 83–95% and specificity of 89–100% for midgut volvulus [14,15,16,17,18]. US is portable, available 24/7 at most institutions, can be interpreted by a remote radiologist, lacks ionizing radiation, and does not require oral contrast agent or enteric tube placement.

In comparison, the upper gastrointestinal (GI) series, which is the current reference standard, has a sensitivity of 54–89% for midgut volvulus [4, 19,20,21]. The upper GI series requires patient transport to the radiology department, administration of oral contrast agent, and use of ionizing radiation. The average effective dose for an upper GI series in a neonate is reported to be 1.6–3.2 mSv [22, 23], with 3 mSv being similar to the dose acquired from a year of natural background radiation in the United States [24, 25]. Furthermore, performing an upper GI series outside of regular hours might require calling a radiologist from home or other remote location and lead to a delay in diagnosis. Given these limitations of the upper GI series, US can serve as an alternative imaging test for diagnosing midgut volvulus.

Ultrasound technique

Probe and position

Imaging can be performed with a high-frequency linear-array probe in neonates and small children and a lower-frequency curved-array probe for larger children and adults. The child lies in supine position and the probe is placed in the subxiphoid region (Fig. 1). Graded compression is used to displace bowel gas as the probe is moved caudally, like the technique used for evaluating the appendix. If gas in the transverse colon cannot be cleared, compression with 45° of caudal angulation of the probe might allow adequate visualization (Fig. 1). The child can be placed in the right lateral decubitus position to move the gas to the left of the abdomen and to facilitate gastric emptying for better visualization of the duodenum. It is important to keep the probe midline and to identify the aorta when evaluating the relationship of the superior mesenteric artery (SMA) and superior mesenteric vein (SMV) to avoid false-positive interpretations (Fig. 2) [26].

Fig. 1
figure 1

Demonstration of probe placement in transverse plane. a The probe is flat or parallel to the surface of the abdomen in the subxiphoid region. b Clinical image shows compression with 45° of caudal angulation of the probe, which might bypass overlying bowel gas, particularly in the transverse colon

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Fig. 2
figure 2

Transverse US image of a 20-day-old girl presenting with projectile vomiting and diagnosis of gastroesophageal reflux. To avoid pitfalls in assessing the relationship of the superior mesenteric artery (SMA) and superior mesenteric vein (SMV) on US, note that the SMV and SMA orientation can vary depending on the probe position. The SMV should normally be to the right of the aorta–SMA axis (line). Ao aorta, IVC inferior vena cava, RK right kidney

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Image acquisition

Gray-scale transverse still images and cine clips of the superior mesenteric vessels from their origin to their branches are crucial in diagnosing midgut malrotation and volvulus. It is recommended to obtain a cine clip of the entire superior mesenteric vascular pedicle, starting from the level of the main portal vein (MPV) to demonstrate the SMA/SMV relationship throughout their course.

The SMA arises from the aorta and has an echogenic collar. The SMV is identified by its confluence with the MPV and splenic vein, ovoid shape, and larger size compared to the SMA (Fig. 2). Color Doppler imaging can help identify swirling of the SMV and mesentery around the SMA (“whirlpool sign”) in the presence of midgut volvulus (Fig. 3).

Fig. 3
figure 3

Classic whirlpool sign can be mistaken for an intussusception on gray-scale US. For example, a 2-year-old boy presented with 5 days of intermittent abdominal pain and watery diarrhea and clinical suspicion of intussusception. About a year earlier, the boy had been diagnosed with gastroesophageal reflux after presenting to the Emergency Department with two episodes of nonbilious vomiting. a, b Transverse gray-scale image (a) and corresponding transverse color Doppler image (b) demonstrate what looks like a target sign in intussusception on a single still image. There was clockwise swirling (curved arrow) of the superior mesenteric vein (SMV) and bowel around the superior mesenteric artery (SMA; straight arrow). With color Doppler, the vascularity makes the whirlpool sign more apparent and confirms the counterclockwise blood flow within the SMV, which is wrapping around the SMA. c, d An upper gastrointestinal (GI) series was requested given the nonspecific clinical findings. Anteroposterior view shows a low-lying duodenojejunal junction (DJJ) relative to the duodenal bulb (arrow in c) and the proximal small bowel remains in the right hemiabdomen (d), compatible with malrotation. Midgut volvulus was not clearly shown in this upper GI series but was confirmed at surgery, underscoring the value of US directly visualizing the twisting of the mesenteric vessels and small bowel

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After visualizing the superior mesenteric vascular pedicle, the next step is to focus on the proximal duodenum and location of the third portion of the duodenum (D3). The normal D3 is retroperitoneal and courses between the proximal SMA and abdominal aorta inferior or anterior to the left renal vein and superior to the origin of the inferior mesenteric artery (Fig. 4) [27]. A cine clip in the transverse plane can be used to depict movement of intraluminal air or fluid through D3, aiding in its identification, and also to confirm that what is suspected to be D3 is connected to the second portion of the duodenum (D2) just lateral to the pancreatic head. Water injected through a nasogastric tube can be used to improve visualization of D3 (Fig. 4) [14, 28, 29]. However, we do not routinely use this technique and have not found it necessary for the diagnosis of most cases of midgut volvulus.

Fig. 4
figure 4

Transverse US images of four children illustrate normal retroperitoneal third portion of the duodenum (D3), which can be seen between the superior mesenteric artery (SMA) and aorta (Ao) at the level of the kidneys. The third portion of the duodenum can have different appearances depending on the degree of intraluminal air or fluid. a A 2-month-old boy with vomiting for 3 days. The boy was diagnosed with vomiting and constipation. Air is noted within the retroperitoneal third portion of the duodenum. SMV superior mesenteric vein. b A 9-day-old boy with trisomy 21 presents with feeding intolerance and diagnosis of duodenal atresia. Here the third portion of the duodenum is completely collapsed. IVC inferior vena cava, RK right kidney, VB vertebral body. c A 23-day-old girl presents with vomiting and diagnosis of gastroesophageal reflux. The third portion of the duodenum is filled with iso- to hyperechoic enteric content. LK left kidney. d An 8-month-old boy with bilious, projectile emesis for 1 week, with small-bowel obstruction secondary to adhesions confirmed at surgery. Fluid dilatation of the third portion of the duodenum, seen posterior to the normally oriented SMA (dashed arrow) and SMV (solid arrow)

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Visualization of the cecum, assisted by identification of the appendix or terminal ileum, in the right lower quadrant supports the presence of normal bowel rotation. However, differentiating large from small bowel and identifying the appendix in a neonate can be challenging. Of note, the cecum of a normally rotated neonate or infant might be positioned in the right upper quadrant because of a lax mesocolon.

How to interpret the findings and avoid pitfalls

Superior mesenteric artery/superior mesenteric vein relationship

The SMV normally lies to the right of the SMA (Fig. 2) [2, 30]. Dufour et al. [31] found that when the SMA/SMV relationship was inverted (i.e. SMV to the left of the SMA), 100% of their patients had midgut malrotation (Fig. 5). When the SMV was anterior or normally located to the right of the SMA, 28% and 3% of those patients had midgut malrotation, respectively [31]. However, Taylor [32] showed that 37% of patients with an inverted SMA/SMV relationship had normal rotation. Therefore, a normal SMA/SMV relationship does not exclude midgut malrotation and an abnormal relationship does not confirm midgut malrotation. The SMA/SMV relationship alone can be misleading when the transverse images are not obtained in the midline [26]. Apart from ensuring proper technique, interpreting the relationship of the SMV to the SMA–aortic axis is a better indicator for normal or abnormal position (Fig. 2) [33]. The finding of an abnormal SMA/SMV relationship along with an intraperitoneal course of D3 are confirmatory of malrotation (Fig. 5). In indeterminate cases in which D3 cannot be visualized, an upper GI series or, depending on patient age and other presenting symptoms, CT or MR might be helpful [34].

Fig. 5
figure 5

Transverse US image shows an inverted relationship of the superior mesenteric artery (SMA) and superior mesenteric vein (SMV) and intraperitoneal third portion of the duodenum (D3) without whirlpool sign in a 1-day-old boy with prenatal history of polyhydramnios and multiple congenital anomalies. These findings are consistent with midgut malrotation without volvulus. At surgery, the boy was found to have duodenal stenosis and malrotation. Ao aorta, LK left kidney, RK right kidney, VB vertebral body

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Whirlpool sign

The clockwise wrapping of bowel, the SMV and the mesentery around the SMA in volvulus complicating midgut malrotation results in the sonographic whirlpool sign (Fig. 3). Shimanuki et al. [13] found that the whirlpool sign had a sensitivity of 92%, specificity of 100% and positive predictive value of 100% for diagnosing midgut volvulus. Three prospective studies had similar results and reported both sensitivity and specificity of 89–96% of the whirlpool sign for midgut volvulus [14, 16, 17]. US can provide the diagnosis of volvulus when the upper GI series does not show the classic corkscrew sign of midgut volvulus because this sign can be subtle, only seen on the lateral view, or absent (Fig. 3) [35]. Therefore, visualization of the whirlpool sign is consistent with midgut malrotation with complicating volvulus and does not require additional confirmatory imaging [16, 36].

A common pitfall is mistaking a counterclockwise course of a jejunal branch of the SMV around the SMA as a whirlpool sign (Fig. 6). This is a normal anatomical variant related to variable branching patterns of the SMV, and it has been well described on CT [32, 37]. Gray-scale cine clips in the craniocaudal direction demonstrate a counterclockwise course of the jejunal vessels branching from the SMV, and on Doppler US the blood flow in the jejunal vein branches demonstrate a clockwise direction as the blood returns to the SMV (Fig. 6). This in contrast to midgut volvulus, in which the SMV typically wraps around the SMA in a clockwise course and Doppler US shows blood returning to the portal vein in a counterclockwise direction (Fig. 3). The whirlpool sign can be subtle (less than 360° twist) or located in the lower abdomen just right or left of midline. Therefore, meticulous evaluation of as much of the course of the superior mesenteric vessels as possible and not just the proximal portions near the level of the pancreas with cine clips might decrease false-negative exams.

Fig. 6
figure 6

Transverse US images in a 10-year-old boy with suspected eosinophilic gastroenteritis presenting with nausea and abdominal pain. The counterclockwise swirling of a vessel branching from the superior mesenteric vein (SMV) can simulate a whirlpool sign and lead to a false-positive exam. a, b Gray-scale image (a) shows a jejunal branch of the SMV and color Doppler image (b) shows a clockwise direction of the blood flow (arrow) in the jejunal vein branch. Compare this with the color Doppler image in Fig. 3, which depicts the classic whirlpool sign of midgut volvulus with SMV blood flow in a counterclockwise direction. SMA superior mesenteric artery

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Ultrasound rarely identifies twisting or volvulus of bowel distant from the superior mesenteric pedicle, not related to intestinal malrotation, as can occur with segmental intestinal volvulus (Fig. 7) and with apple-peel intestinal atresia [38].

Fig. 7
figure 7

Segmental volvulus of the ileum without midgut malrotation in a 1-day-old girl with suspected in utero bowel perforation. a Transverse US image shows a normal relationship of the superior mesenteric artery (dashed arrow) and superior mesenteric vein (solid arrow) and a normal course of the duodenum portions 1 through 3 (D1, D2, D3), including the retroperitoneal position of the third portion of the duodenum (D3), consistent with normal midgut rotation. Star indicates complex ascites. Ao aorta. b Transverse US image of the right lower quadrant shows a twisted loop of bowel (curved arrow), which was confirmed at surgery to represent segmental volvulus of the ileum leading to necrosis and perforation. Additional findings of in utero bowel obstruction and perforation include dilated small bowel with a fluid-fluid level (straight arrow) and complex ascites (star)

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Duodenal dilatation

The normal duodenum is typically collapsed or mildly distended with fluid and air (Fig. 8). Obstruction of the duodenum by the volvulus often results in proximal dilatation, sometimes with layering enteric debris (Fig. 9) or to-and-fro motion of the intraluminal contents of the proximal duodenum, which is best seen on cline clips. Duodenal dilatation with distal tapering of D3 (Fig. 9) has a sensitivity of 89% and specificity of 92% for midgut volvulus [14]. The finding of a dilated first duodenal portion (D1), D2 or proximal D3 warrants meticulous investigation for other findings of midgut volvulus, including a whirlpool sign, which might be subtle (Fig. 9).

Fig. 8
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Transverse US image shows normal pylorus (P) and normal first portion of the duodenum (D1) and second portion of the duodenum (D2) in a 9-day-old girl who presented with vomiting and diagnosis of gastroesophageal reflux

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Fig. 9
figure 9

Dilatation of the stomach, pylorus (P) and first and second portions of the duodenum (D1 and D2) should alert the ultrasonographer or radiologist to meticulously evaluate for an underlying cause. a Transverse image in a 1-month-old girl with two episodes of bilious emesis. US was performed and initially interpreted as normal, but upon further evaluation, the proximal duodenum (D1 and D2) is dilated, raising the suspicion of a proximal small-bowel obstruction. RK right kidney. b When imaged more caudally in the transverse plane, there is tapering or beaking of the third portion of the duodenum (D3; sideways V) as it is pulled intraperitoneally anterior to the superior mesenteric artery, forming a subtle whirlpool sign (arrow) just to the left of midline. At surgery, midgut volvulus was found. There was bowel ischemia, which improved following untwisting

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Duodenal dilatation can result from other causes of duodenal obstruction in addition to midgut volvulus or Ladd bands, complicating malrotation; these other causes include congenital anomalies such as annular pancreas (Fig. 10), duodenal atresia (Fig. 11), stenosis or web, as well as acquired conditions such as duodenal hematoma. Distinction among these conditions is important to guide the urgency of corrective surgery. US can play a crucial role in this regard because upper GI series might not allow for differentiation of duodenal atresia from midgut volvulus if enteric contrast agent does not progress past D2 (Fig. 11). Recognition on US of a thickened (≥2 mm) and echogenic bowel wall of the stomach and duodenum in the presence of a normal SMA/SMV relationship and position of D3 favors the diagnosis of duodenal atresia (Fig. 11) [39]. On the other hand, beaking of D3 just before it gets pulled into the whirlpool sign confirms midgut malrotation with complicating volvulus (Fig. 9).

Fig. 10
figure 10

Malrotation can coexist with other congenital malformations such as annular pancreas, as seen in this 3-day-old girl with bilious emesis. a Transverse US scan shows inversion of the relationship of the superior mesenteric artery (SMA) and superior mesenteric vein (SMV). The third portion of the duodenum (D3) does not cross to the left anterior to the aorta (Ao). No whirlpool sign was identified. These findings are consistent with malrotation without volvulus. IVC inferior vena cava, RK right kidney. b Transverse US image shows echogenic pancreatic tissue (asterisks) extending beyond the head of the pancreas and wrapping around the second portion of the duodenum (D2). c Transverse US image shows collapsed bowel in the right hemiabdomen, supporting the diagnosis of midgut malrotation. Surgery confirmed midgut malrotation with annular pancreas

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Fig. 11
figure 11

Dilatation of stomach and proximal duodenum caused by duodenal atresia without malrotation in a 5-day-old girl presenting with brown emesis. a Transverse US image shows normal relationship of the superior mesenteric artery (SMA) and superior mesenteric vein (SMV) without whirlpool sign and a collapsed retroperitoneal third portion of the duodenum (D3) coursing between the aorta (Ao) and the SMA, compatible with normal bowel rotation. There is wall thickening of the first portion of the duodenum (D1; asterisk), which favors the diagnosis of duodenal atresia over midgut malrotation. D2 second portion of the duodenum. b Oblique image from a subsequent upper gastrointestinal series shows beaking (solid arrow) of the second portion of the duodenum without contrast agent progressing distally. Air seen distally (dashed arrow) is likely from a coexisting biliary tree anomaly allowing for air to bypass the atretic portion of the duodenum via an anomalous biliary connection. Surgery confirmed duodenal atresia without midgut malrotation

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Although dilated proximal duodenum can be a clue for obstruction from midgut volvulus, such dilatation might be absent because of decompression by an enteric tube or from recent or recurrent emesis (Fig. 12).

Fig. 12
figure 12

Midgut volvulus without dilatation of the stomach or proximal duodenum in a 7-day-old boy with bilious emesis. a Transverse US image shows a nondilated stomach and the first (D1) and second (D2) portions of the duodenum, which can occur in midgut volvulus either from decompression by an enteric tube or, in the case of this child, from persistent vomiting. The absence of proximal dilatation does not exclude and should not deter one from searching for midgut malrotation or volvulus. Ao aorta, Asterisk portosplenic confluence, IVC inferior vena cava. b Transverse US image just caudal to (a) shows a subtle whirlpool sign (arrow), consistent with midgut volvulus. Surgery showed a 360° midgut volvulus with an internal hernia

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Position of the third portion of the duodenum (D3)

D3 is retroperitoneal in children with normal midgut rotation [40]. D3 normally courses leftward immediately anterior to the abdominal aorta between the proximal SMA and aorta superior to the origin of the inferior mesenteric artery, inferior to the splenic vein and anterior or inferior to the renal veins [27, 40]. Without knowledge of the appropriate anatomy, other loops of small bowel can be mistaken for a normal retroperitoneal D3, leading to a false-negative exam. Yousefzadeh et al. [27] reported that the normal D3 was reliably visualized by US in 33 of 33 newborns and was characterized by crossing midline to the left side and having gut signature, fluid or air contents, and an anteroposterior (AP) dimension of 2–9 mm (Fig. 4). Given that a collapsed D3 can measure only 2 mm in anteroposterior (AP) dimension and be obscured by overlying bowel gas, identifying it can be challenging. Instilling water through a nasogastric tube might help in the identification of D3 [14, 28, 29]. Despite the challenges, the mean time for Khatami et al. [41] to identify D3 in 60 of 60 newborns and infants was 48 s. These US exams were performed without any bowel preparation or sedatives [41]. False-negative exams based on D3 positioning rarely occur; Taylor [32] reported a retroperitoneal appearance of D3 in 1 of 38 patients with midgut malrotation on CT. It is unclear whether this one patient had other signs such as an abnormal SMA and SMV relationship or abnormal position of the cecum that would have raised the suspicion of malrotation.

Interpretation of the sonographic findings (from ‘findings’ to ‘impression’)

To best assist referring physicians in patient management, the report impression might be structured to provide a diagnosis, level of confidence in that diagnosis, and recommendations for additional imaging, if appropriate. Intraperitoneal D3 is diagnostic of midgut malrotation. An abnormal SMA and SMV relationship suggests midgut malrotation if D3 is not visualized and should be correlated with symptoms and an upper GI series or other imaging as clinically appropriate. A whirlpool sign is diagnostic of volvulus. The findings of proximal duodenal dilatation with a tapered configuration and an abnormal SMA/SMV relationship or intraperitoneal D3 is diagnostic of midgut malrotation with volvulus or obstructing Ladd bands. Proximal duodenal dilatation in the absence of signs of midgut malrotation or a whirlpool sign suggests duodenal obstruction by an atresia, web, stenosis, annular pancreas or hematoma. A retroperitoneal D3 with a normal SMA/SMV relationship in practice excludes malrotation.

Conclusion

The diagnosis of volvulus complicating midgut malrotation can usually be confidently made based on US findings. Adherence to proper technique, recognition of salient findings, and awareness of potential pitfalls are essential to avoid delayed diagnosis from false-negative exams and unnecessary surgery from false-positive exams.